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Transcription and Mrna Processing Get Even Closer View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Cell, Vol. 120, 163–166, January 28, 2005, Copyright ©2005 by Elsevier Inc. DOI 10.1016/j.cell.2005.01.002 The Spanish Connection: Meeting Review Transcription and mRNA Processing Get Even Closer Manuel Ares, Jr.1,* and Nick J. Proudfoot2,* place before elongation can fully proceed (Figure 1A). 1Department of Molecular Cell At early elongation, the C-terminal domain (CTD) of the and Developmental Biology Pol II large subunit (Rpb1) becomes phosphorylated on University of California, Santa Cruz serine 5 positions within its characteristic heptad re- Santa Cruz, California 95064 peats. Ser5 phosphorylation at CTD recruits the mRNA 2Sir William Dunn School of Pathology capping complex, which adds a cap to the initial nascent University of Oxford transcript. Ser5 phosphorylation is also associated with South Parks Road specific nucleosomal marks at the 5Ј end of the gene, Oxford OX1 3RE such as histone H3 lysine 4 trimethylation (Hampsey United Kingdom and Reinberg, 2003). Several presentations dwelt on new aspects of cou- pling during early transcription elongation. John Lis (Cornell University, New York) described the presence The synthesis of mRNA by RNA polymerase II appears of the elongation factor TFIIS on RNA polymerase II that coupled to numerous RNA-processing events, based is paused at the beginning of Drosophila heat shock on physical or functional connections revealed by bio- genes prior to heat induction. During normal elongation, chemical or genetic tests. New findings were pre- TFIIS is thought to promote cleavage of those tran- sented at a recent meeting in Spain that begin to illumi- scripts whose 3Ј ends are misaligned in the polymerase nate the mechanisms underlying the connections active site, thus allowing polymerase to escape tran- between mRNA processing and specific steps in tran- script arrest (Fish and Kane, 2002). A similar scenario scription (initiation, elongation, and termination) as now appears to operate at the heat shock genes where well as recombination. TFIIS-stimulated transcript cleavage is required to allow the stalled Pol II to resume elongation following heat The production of functional messenger RNA in eukary- shock activation (Adelman et al., 2005). Danny Reinberg otes requires not only transcript synthesis by RNA poly- (University of Medicine and Dentistry of New Jersey, merase II (Pol II) but also multiple RNA-processing steps New Jersey) described biochemical analysis of a large such as capping, splicing, polyadenylation, and RNA complex containing both elongation and chromatin re- editing. Recent research has shown that many of these modeling factors. Components of this complex specifi- processing steps occur cotranscriptionally, revealing a cally associate with Lys4 trimethylated histone H3, a close association (coupling) between transcription and well-known histone modification found at the transcrip- mRNA processing (Proudfoot et al., 2002). At a recent tion start site (Ng et al., 2003). Interestingly, this complex meeting in Spain (November 7–10, 2004), new findings significantly stimulates in vitro splicing reactions, as were presented that begin to clarify the connections shown by a collaborative experiment with the laboratory between transcription (initiation, elongation, and termi- of Jim Manley (Columbia University, New York). These nation) and messenger RNA processing and even re- results raise the possibility that recruitment of this com- combination. The meeting, titled “Coupling between plex during early elongation may facilitate subsequent Transcription and RNA Processing” and organized by splicing reactions that occur cotranscriptionally. Miguel Beato and Juan Valcarcel, was hosted by the Universidad Internacional de Andalucia at the Sede An- Packaging mRNA into mRNPs during Elongation: tonio Machado, a restored 17th century palace in Baeza, The R Loop Story site of a Renaissance university in the south of Spain. It has long been known that pre-mRNA is packaged into The intimate setting and small size of the meeting suc- protein-associated complexes (mRNPs, originally called cessfully encouraged open discussion. A shared goal of hnRNPs) that contain both general nuclear proteins such the participants was to learn more about the molecular as hnRNP A (and other family members) and more spe- mechanisms coupling transcription and RNA pro- cific splicing/mRNA export-associated protein factors cessing. Such connections are already in part defined by such as the THO/TREX complex (Jensen et al., 2003). protein-protein or protein-nucleic acid interaction data While this packaging process is well known to be re- using either biochemical or genetic tests. However, the quired for mRNA maturation, it also appears to be re- precise mechanisms by which coupling occurs remain quired for protection of the integrity of the DNA template largely mysterious. itself. New findings were presented on the intriguing phenomenon of transcription-dependent hyperrecom- bination, which is stimulated by defects in elongation Early Elongation Coupling factors or in mRNA export. Recently published studies Once Pol II has escaped from a gene promoter into early in yeast from Andres Aguilera’s lab (University of Seville, elongation, a number of molecular events appear to take Spain; Huertas and Aguilera, 2003) suggested a provoc- ative model in which, if the nascent RNA emerging from Pol II is not immediately and properly coated by mRNP *Correspondence: [email protected] (M.A.); nicholas.proudfoot@ packaging proteins, then it will result in the formation pathology.oxford.ac.uk (N.J.P.) of an R loop with underwound DNA located just behind Cell 164 Figure 1. Cartoons Depicting Four Stages in the Coupling of Pol II Transcription with Pre-mRNA Processing See text for full details. (A) Elongating Pol II may be poised at the start of the gene with its CTD heptad repeats in a serine 5-phosphorylated state and the nucleosomes marked by histone H3 lysine 4 trimethylation (H3-K4 trimethylation). The involvement of TFIIS and the capping complex is indicated. (B) Deficient pre-mRNA packaging may result in topological pausing of elongating Pol II through the formation of pre-mRNA:DNA R loops. The looped-out sense DNA strand is then susceptible to DNA damage by hyperrecombination. R loops may be relieved by RNase H activity. (C) Pre-mRNA is cotranscriptionally packaged, spliced, and edited during elongation. Nucleosomes are also repositioned on the DNA chromatin template during elongation. (D) Termination of Pol II transcription. Cleavage and polyadenylation at the 3Ј end of the pre-mRNA is mediated by cleavage/polyadenylation factors. The downstream transcript that remains attached to the elongating Pol II is then subjected to 5Ј-3Ј exonucleolytic degradation, eventually leading to the release of Pol II from the DNA template. the elongating polymerase (Figure 1B). This in turn leads elongation. Jensen showed that mutations in elongation to both impairment of transcription and a hyperrecombi- factors such as Rad3 (a subunit of TFIIH) and Dst1 (a nation phenotype restricted to the transcribed locus. homolog of mammalian TFIIS) mitigated the transcrip- Now Jim Manley’s group reports the unexpected finding tion elongation defect caused by mutations in the THO that genetic inactivation of the SR protein splicing factor complex, suggesting that the inadequacy of mRNP pack- ASF/SF2 in chicken DT40 cells (Wang et al., 1998) results aging caused by lack of THO is more pronounced when in a similar phenotype. This new study highlights the transcription elongation proceeds at a higher rate (Jen- critical importance of properly integrating transcription sen et al., 2004). On a related theme, he also showed that with the correct processing of the nascent transcript. THO defects appear to adversely affect later elongation Together, these findings bolster the hypothesis that de- stages, causing apparent premature termination. Similar fective packaging of the nascent transcript leads to R observations were also made in the Aguilera lab. Manny loop formation behind the polymerase, which stimulates Ares (University of Santa Cruz, California) reported on recombination and may also drag the elongating poly- experiments with Grant Hartzog’s lab in which they merase to a halt. found that yeast cells carrying mutations in genes for The contribution of nascent RNA packaging to elonga- THO/TREX/, PAF, and FACT complex subunits share tion was further illuminated by exciting data from Andres highly similar genome-wide reduction in pre-mRNA and Aguilera and Torben Heick Jensen (Aarhus University, mRNA levels. Both PAF and FACT are chromatin-associ- Denmark). They both described experiments illustrating ated elongation factors (Hampsey and Reinberg, 2003; the effect of THO complex mutations on transcription Belotserkovskaya et al., 2003). This is consistent with Review 165 the notion that compromising the function of proteins Attempts to capture the synchronicity of transcription involved in mRNA packaging and elongation leads to and splicing events in vivo using chromatin crosslinking common downstream defects in gene expression (Bur- of splicing factors continue to move forward in yeast, ckin et al., 2005). All of these results suggest that, in following on the initial finding that the U1 snRNP is the absence of efficient mRNP packaging, topological cotranscriptionally recruited to intron-containing genes problems
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